Pathways involved in the generation of reactive oxygen and nitrogen species during glucose deprivation and its role on the death of cultured hippocampal neurons

Neuroscience

Volumn 167, Issue 4, 2010, Pages 1057-1069

  Paramo B ^a   Hernandez Fonseca K ^a   Estrada Sanchez A M ^a   Jimenez N ^a   Hernandez Cruz A ^a   Massieu, L ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Excitotoxicity; Hypoglycemia; NADPH oxidase; Oxidative damage; Xanthine oxidase

Indexed keywords

EBSELEN; GLUCOSE; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE SYNTHASE; PHOSPHOLIPASE A2; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; TROLOX C; XANTHINE OXIDASE;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL DEATH; CONTROLLED STUDY; EMBRYO; EXCITOTOXICITY; HIPPOCAMPUS; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

EID: 77952554583     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.02.074     Document Type: Article

References (49)

1. Abramov A.Y., Scorziello A., Duchen M.R. Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. J Neurosci 2007, 275:1129-1138.
2. Arai K., Ikegaya Y., Nakatani Y., Kudo I., Nishiyama N., Matsuki N. Phospholipase A2 mediates ischemic injury in the hippocampus: a regional difference of neuronal vulnerability. Eur J Neurosci 2001, 13:2319-2323.
3. Auer R.N., Olsson Y., Siesjö B.K. Hypoglycemic brain injury in the rat. Correlation of density of brain damage with the EEG isoelectric time: a quantitative study. Diabetes 1984, 33:1090-1098.
4. Auer R.N., Wieloch T., Olsson Y., Siesjö B.K. The distribution of hypoglycemic brain damage. Acta Neuropathol 1984, 64:177-191.
5. Babbedge R.C., Bland-Ward P.A., Hart S.L., Moore P.K. Inhibition of rat cerebellar nitric oxide synthase by 7-nitro indazole and related substituted indazoles. Br J Pharmacol 1993, 110:225-228.
6. Bergmeyer H.U., Bernt E.H. Methods of enzymatic analysis 1968, 736-741. Academic Press, New York.
7. Berridge M.V., Tan A.S. Characterization of the cellular reduction of 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction. Arch Biochem Biophys 1993, 303:474-482.
8. Bindokas V., Jordan J., Lee C., Miller R. Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J Neurosci 1996, 16:1324-1336.
9. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
10. Brennan A.M., Suh S.W., Won S.J., Narasimhan P., Kauppinen T.M., Lee H., Edling Y., Chan P.H., Swanson R.A. NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat Neurosci 2009, 12:857-863.
11. Brewer G.J., Torricelli J.R., Evege E.K., Price P.J. Optimized survival of hippocampal neurons in B27-suplemented neurobasal, a new serum free medium combination. J Neurosci Res 1993, 35:567-576.
12. Chow H.S., Lynch J.J., Rose K., Choi D.W. Trolox attenuates cortical neuronal injury induced by iron, ultraviolet light, glucose deprivation, or AMPA. Brain Res 1994, 639:102-108.
13. Ennis K., Tran P.V., Seaquist E.R., Rao R. Postnatal age influences hypoglycemia-induced neuronal injury in the rat brain. Brain Res 2008, 1224:119-126.
14. Estrada-Sánchez A.M., Camacho A., Montiel T., Massieu L. Cerebellar granule neurons are more vulnerable to transient transport-mediated glutamate release than to glutamate uptake blockade. Correlation with excitatory amino acids levels. Neurochem Res 2007, 32:423-432.
15. Floriano-Sánchez E., Villanueva C., Medina-Campos O.N., Rocha D., Sánchez-Gonzalez D.J., Cardenas-Rodriguez N., Pedraza-Chaverri J. Nordihydroguaiaretic acid is a potent in vitro scavenger of peroxynitrite, singlet oxygen, hydroxyl radical, superoxide anion and hypochlorous acid and prevents in vivo ozone-induced tyrosine nitration in lungs. Free Radic Res 2006, 40:523-533.
16. Garvey E.P., Oplinger J.A., Tanoury G.J., Sherman P.A., Fowler M., Marshall S., Harmon M.F., Paith J.E., Furfine E.S. Potent and selective inhibition of human nitric oxide synthases. Inhibition by non-amino acid isothioureas. J Biol Chem 1994, 269:26669-26676.
17. Gomes A., Fernandes E., Lima J.L. Fluorescence probes used for detection of reactive oxygen species. J Biochem Biophys Methods 2005, 65:45-80.
18. Haces M.L., Hernández-Fonseca K., Medina-Campos O.N., Montiel T., Pedraza-Chaverri J., Massieu L. Antioxidant capacity contributes to protection of ketone bodies against oxidative damage induced during hypoglycemic conditions. Exp Neurol 2008, 211:85-96.
19. Haces M.L., Montiel T., Massieu L. Selective vulnerability of brain regions to oxidative stress in a non-coma model of insulin-induced hypoglycemia. Neuroscience 2010, 165:28-38.
20. Hernández-Fonseca K., Cárdenas-Rodríguez N., Pedraza-Chaverri J., Massieu L. Calcium-dependent production of reactive oxygen species is involved in neuronal damage induced during glycolysis inhibition in cultured hippocampal neurons. J Neurosci Res 2008, 86:1768-1780.
21. Hernández-Fonseca K., Massieu L. Disruption of endoplasmic reticulum calcium stores is involved in neuronal death induced by glycolysis inhibition in cultured hippocampal neurons. J Neurosci Res 2005, 82:196-205.
22. Hockenbery D.M., Oltvai Z.N., Yin X.M., Milliman C.L., Korsmeyer S.J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 1993, 75:241-251.
23. Isaev N.K., Stelmashook E.V., Dirnagl U., Plotnikov E.Y., Kuvshinova E.A., Zorov D.B. Mitochondrial free radical production induced by glucose deprivation in cerebellar granule neurons. Biochemistry Mosc 2008, 73:149-155.
24. Kalimo H., Auer R.N., Siesjö B.K. The temporal evolution of hypoglycemic brain damage. III. Light and electron microscopic findings in the rat caudoputamen. Acta Neuropathol 1985, 67:37-50.
25. Kishida K.T., Pao M., Holland S.M., Klann E. NADPH oxidase is required for NMDA receptor-dependent activation of ERK in hippocampal area CA1. J Neurochem 2005, 94:299-306.
26. Lin Y., Phillis J.W. Oxypurinol reduces focal ischemic brain injury in the rat. Neurosci Lett 1991, 126:187-190.
27. Maiorino M., Roveri A., Ursini F. Antioxidant effect of ebselen (PZ 51): peroxidase mimetic activity on phospholipid and cholesterol hydroperoxides vs free radical scavenger activity. Arch Biochem Biophys 1988, 295:404-409.
28. McGowan J.E., Chen L., Gao D., Trush M., Wei C. Increased mitochondrial reactive oxygen species production in newborn brain during hypoglycemia. Neurosci Lett 2006, 399:111-114.
29. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983, 65:55-63.
30. Müller A., Cadenas E., Graf P., Sies H. A novel biologically active seleno-organic compound. I. Glutathione peroxidase-like activity in-vitro and antioxidant capacity of PZ 51 (ebselen). Biochem Pharmacol 1984, 33:3235-3239.
31. Nagasawa K., Kakuda T., Higashi Y., Fujimoto S. Possible involvement of 12-lipoxygenase activation in glucose-deprivation/reload-treated neurons. Neurosci Lett 2007, 429:120-125.
32. Nakane M., Klinghofer V., Kuk J.E., Donnelly J.L., Budzik G.P., Pollock J.S., Basha F., Carter G.W. Novel potent and selective inhibitors of inducible nitric oxide synthase. Mol Pharmacol 1995, 47:831-834.
33. Nanda B.L., Nataraju A., Rajesh R., Rangappa K.S., Shekar M.A., Vishwanath B.S. PLA2 mediated arachidonate free radicals: PLA2 inhibition and neutralization of free radicals by anti-oxidants-a new role as anti-inflammatory molecule. Curr Top Med Chem 2007, 7:765-777.
34. Owada Y., Tominaga T., Yoshimoto T., Kondo H. Molecular cloning of rat cDNA for cytosolic phospholipase A2 and the increased gene expression in the dentate gyrus following transient forebrain ischemia. Mol Brain Res 1994, 25:364-368.
35. Papadopoulus M.C., Koumenis I.L., Dugan L.L., Giffard R.G. Vulnerability of glucose deprivation injury correlates with glutathione levels in astrocytes. Brain Res 1997, 748:151-156.
36. Patočková J., Marhol P., Tumova E., Krsiak M., Rokyta R., Stipek S., Crkovska J., Andel M. Oxidative stress in the brain tissue of laboratory mice with acute post insulin hypoglycemia. Physiol Res 2003, 52:131-135.
37. Rego A.C., Santos M.S., Oliveira C.R. Influence of the antioxidants vitamin E and idebenone on retinal cell injury mediated by chemical ischemia, hypoglycemia, or oxidative stress. Free Radic Biol Med 1999, 26:1405-1407.
38. Robinson K.M., Janes M.S., Pehar M., Monette J.S., Ross M.F., Hagen T.M., Murphy M.P., Beckman J.S. Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc Natl Acad Sci U S A 2006, 103:15038-15043.
39. Saluja I., Song D., Oregan M.H., Phillis J.W. Role of phospholipase A2 in the release of free fatty acids during ischemia-reperfusion in the rat cerebral cortex. Neurosci Lett 1997, 233:97-100.
40. Sandberg M., Butcher S.T., Hagberg H. Extracellular overflow of neuroactive amino acids during severe insulin-induced hypoglycemia: in vivo dialysis of the rat hippocampus. J Neurochem 1986, 47:178-184.
41. Schewe T. Molecular actions of ebselen-an anti-inflamatory antioxidant. Gen Pharmacol 1995, 26:1153-1169.
42. Shelat P.B., Chalimoniuk M., Wang J.H., Strosznajder J.B., Lee J.C., Sun A.Y., Simonyi A., Sun G.Y. Amyloid beta peptide and NMDA induce ROS from NADPH oxidase and AA release from cytosolic phospholipase A2 in cortical neurons. J Neurochem 2008, 106:45-55.
43. Southan G.J., Szabó C., Thiemermann C. Isothioureas: potent inhibitors of nitric oxide synthases with variable isoform selectivity. Br J Pharmacol 1995, 114:510-516.
44. Suh S.W., Aoyama K., Chen Y., Garnier P., Matsumori Y., Gum E., Liu J., Swanson R.A. Hypoglycemic neuronal death and cognitive impairment are prevented by poly(ADP-ribose) polymerase inhibitors administered after hypoglycemia. J Neurosci 2003, 23:10681-10690.
45. Suh S.W., Gum E., Hamby A.M., Chan P.H., Swanson R.A. Hypoglycemic neuronal death is triggered by glucose reperfusion and activation of neuronal NADPH oxidase. J Clin Invest 2007, 117:910-918.
46. Suh S.W., Hamby A.M., Gum E.T., Shin B.S., Won S.J., Sheline C.T., Chan P.H., Swanson R.A. Sequential release of nitric oxide, zinc, and superoxide in hypoglycemic neuronal death. J Cereb Blood Flow Metab 2008, 28:1697-1706.
47. Tkacs N.C., Pan Y., Raghupathi R., Dunn-Meynell A.A., Levin B.E. Cortical Fluoro-Jade staining and blunted adrenomedullary response to hypoglycemia after noncoma hypoglycemia in rats. J Cereb Blood Flow Metab 2005, 25:1645-1655.
48. Wieloch T. Hypoglycemia-induced neuronal damage prevented by an N-methyl-d-aspartate antagonist. Science 1984, 230:681-683.
49. Zhao H., Kalivendi S., Zhang H., Joseph J., Nithipatikom K., Vasquez-Vivar J., Kalyanaraman B. Superoxide reacts with hydroethidine but forms a fluorescent product that is distinctly different from ethidium: potential implications in intracellular fluorescence detection of superoxide. Free Radic Biol Med 2003, 34:1359-1368.